Abstract

To investigate the consequences of hybridization between species, we studied three replicate hybrid populations that formed naturally between two swordtail fish species, estimating their fine-scale genetic map and inferring ancestry along the genomes of 690 individuals. In all three populations, ancestry from the "minor" parental species is more common in regions of high recombination and where there is linkage to fewer putative targets of selection. The same patterns are apparent in a reanalysis of human and archaic admixture. These results support models in which ancestry from the minor parental species is more likely to persist when rapidly uncoupled from alleles that are deleterious in hybrids. Our analyses further indicate that selection on swordtail hybrids stems predominantly from deleterious combinations of epistatically interacting alleles.

(A) In the presence of hybrid incompatibilities, minor parent ancestry is more likely to persist in regions of high recombination. (B) Shown is one, randomly-chosen replicate of simulations under plausible parameters for swordtail species (). (C) Relationship between minor parent ancestry and recombination rate in swordtails and (D) in humans (see ). Data are summarized in 50 kb windows in swordtail analyses and 250 kb in humans, so that the number of windows is similar. (E) Spearman’s correlations between average minor parent ancestry and recombination rate at several scales; see for complete results and 25 for details of the Denisovan analysis. In B–D, red points and whiskers indicate the mean with two standard errors of the mean determined by bootstrapping; gray points show raw data. Quantile binning is for visualization; statistical tests were performed on the unbinned data.

(A) Maximum likelihood trees from RAxML for 1,000 alignments of randomly selected 10 kb regions. Dxy refers to the average nucleotide divergence between X. birchmanni and X. malinche. (B) Locations of hybrid populations in river systems in Hidalgo, Mexico; listed in blue are elevations of the hybrid populations and typical elevations for parental populations. (C) Inferred ancestry proportions of individuals from each population. (D) Effective population sizes inferred from three X. malinche genomes (sampled from two populations) and 20 X. birchmanni genomes; 50 bootstraps are shown for one individual from each X. malinche population ().

(A, B) Correlations in ancestry between independently formed swordtail hybrid populations (in 0.1 cM windows; ). Points show the mean and whiskers indicate two standard errors of the mean; correlations are calculated on unbinned data. (C) Predictions for different sources of selection on hybrids. (D) Average minor parent ancestry is unusually depleted in 50 kb windows containing putative unlinked BDMIs (red points, from ) compared to 1,000 null datasets (blue; see ). Importantly, low minor parent ancestry at putative BDMIs is not expected as a result of how they were originally identified ().

The recombination mechanism shapes the distribution of minor parent ancestry

(A) Neanderthal ancestry is not elevated in 50 kb windows that overlap with CpG islands (CGIs), when compared to windows that do not, but have similar GC content. The fold difference λ is 0.95 (p=0.91; see ). The same analysis in swordtail hybrids reveals that minor parent ancestry is higher in windows that overlap CGIs (pop. 1, λ=1.09, p<0.005; pop. 2, λ=1.09, p<0.005; pop. 3, λ=1.02, p<0.005). Points show the mean and whiskers indicate two standard errors of the mean obtained by 1,000 joint bootstraps. (B) Simulations of incompatibility selection in swordtails predict higher minor parent ancestry near CGIs. (C) This prediction is met for all hybrid populations. In B and C, gray lines show results of 500 replicate simulations bootstrapping 5 kb windows; colored lines indicate the mean of all replicates in sliding 5 kb windows.